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Lower learning abilities in stereotypic horses
Applied Animal Behaviour Science 107 (2007) 299–306 www.elsevier.com/locate/applanim
Lower learning abilities in stereotypic horses Martine Hausberger *, Emmanuel Gautier, Christine Mu¨ller, Patrick Jego UMR 6552 CNRS Ethologie, Evolution, Ecologie, Universite´ de Rennes 1, Campus de Beaulieu, 35042 Rennes Cedex, France Accepted 5 October 2006 Available online 13 November 2006
Abstract The question of whether motor stereotypies may be associated with learning disorders is a highly debated issue both in humans and animals, but evidence is still scarce. The aim of the present study was to investigate the relation between the occurrence of stereotypic behaviours in horses where stereotypies are well described and learning abilities measurable. Seventy horses were observed in their box at two periods (August and November) and were then submitted to an instrumental task (opening a chest by raising the lid using the nose). Fifty-one of them had shown stereotypic behaviours at both periods. It appeared that more stereotypic horses (36/51) were unsuccessful than non-stereotypic horses (3/19) in the learning task. When successful, they required a longer time in order to perform the task (368 s on average against 220 for the nonstereotypic horses). No difference was found according to the type of stereotypy performed. This is to our knowledge the first time that a relation is found between stereotypy and learning in an animal species. The additional finding that stereotypic horses spent less time lying down and sleeping suggests a possible role of attentional processes. This finding has important implications for the horse industry. # 2006 Published by Elsevier B.V. Keywords: Stereotypies; Learning ability; Horses
1. Introduction The question of whether motor stereotypies may be associated with learning disorders is a highly debated issue, especially in humans, but evidence is still scarce. Mahone et al. (2004) found that 20% of children with motor complex stereotypies exhibited a learning disability. * Corresponding author. Tel.: +33 2 23 23 69 28; fax: +33 2 23 23 69 27. E-mail address: [email protected] (M. Hausberger). 0168-1591/$ – see front matter # 2006 Published by Elsevier B.V. doi:10.1016/j.applanim.2006.10.003
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Patients with Tourette syndrome show learning disabilities (Burd et al., 1992; Marsh et al., 2004) as a result of basal ganglia deficits (Fattaposta et al., 2005; Singer, 2005). However to what extent motor and learning disorders are related remains an important issue. The development of animal models would certainly lead to a better understanding of these phenomena (Marsh et al., 2004), but evidence is scarce here too. The existence of motor disorders, commonly called stereotypies, is well known in captive and ¨ dberg, 1986; Cooper and Nicol, 1996; Wu¨rbel et al., 1996; domestic animals: rodents, birds (O Powell et al., 1999; Callard et al., 2000) but also farm animals (cattle: Redbo, 1993, 1998; pigs: Cronin et al., 1985; Rushen et al., 1990; Wiepkema and Schouten, 1992). This phenomenon receives particular attention in horses, as these behaviours are undesirable for owners and may lead to physiological problems. In horses, repetive movements without any specific goal have been defined as stereotypies (Houpt and McDonnell, 1993), obsessive-compulsive or compulsive disorders (Luescher et al., 1991, 1998; review in Mills, 2005). They tend to appear in unfavourable conditions (McGreevy et al., 1995) in predisposed animals (Hausberger and Richard, 2005). Stereotypies tend to be associated with higher endorphin levels (McGreevy and Nicol, 1998; Pell and McGreevy, 1999). Whether or not learning abilities or performance are impaired in these animals is not known (Mills, 2005). In the present study, we investigated the relation between the occurrence of stereotypic behaviours in individual horses and their ability to learn a task. Observations of the behaviour of 70 horses in their box let us identify ‘‘stable stereotypic’’ horses (stereotypies were present both in two periods separated by a 3 month interval) and non-stereotypic horses. We then submitted both categories of horses to a learning test that correlates with learning abilities in the working situation (Le Scolan et al., 1997). 2. Materials and methods 2.1. Animals and observation procedures Seventy seven French saddlebred horses were observed at the ‘‘Ecole Nationale d’Equitation’’ at Saumur (France) at two time periods: August and November. They were 4–15-year old geldings and were all housed in the same conditions: single box housing (3.30 m 3.40 m), 1 h riding everyday (see Table 1). They were fed pellets and hay twice a day and had water ad libitum. Only the animals that showed stereotypic (or no stereotypic) behaviour consistently at the two time periods were kept for the study, which corresponded to 70 horses. The seven others were only performing stereotypies in November. The analyses included evaluations of individual stereotypies and an analysis of pooled data. Horses were observed in their box using two different methods, with the aim of ensuring that the animal really belonged to one or the other category: Table 1 Type of work performed by the horses observed in their box and tested in the learning task (number of horses)
All horses Stereotypic
Jumping
Eventing
Instruction
Voltige
Dressage
High school
21 16
8 3
12 7
5 2
20 15
11 8
High school horses are dressage horses at a more sophisticated level of performance (elevated paces). The work of the voltige horses differs from the other categories: the horses are lunged on a circle and the riders jump on the back and perform gymnastic movements.
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In the August session, focal sampling was used: all behaviours of the focal animal were recorded continuously during sessions of 5 min. Observations were made at three time periods: 8–11 a.m., 1–4 p.m. and 5–7 p.m. Meals were distributed between 6.30 and 7 a.m. and 4.15–6.30 p.m. All horses were observed 10 times (=50 min total/horse), covering the three daily sessions that included time periods before and after the meals (favourable for observing repetitive movements: Cooper et al., 2000; Mills and Macleod, 2002). In the November session, observations were made using instantaneous scan sampling (Altman, 1974): each horse was observed in sessions of 5 min with behaviour being recorded every 10 s. Each horse was observed four times at the same daily periods as in August. A total of 120 scans were obtained for each horse (20 min). All observations in the box were made by a single observer. To control for differences in learning abilities between (dressage + high school) and (eventing + jumping) horses (Hausberger et al., 2004), the ratio of stereotypic horses was approximately equal in each category (23/31 and 19/29). 2.2. Terminology The stereotypic behaviours noted corresponded to those described in a variety of studies (review in Mills, 2005) and had the common feature of consisting of minor repetitive movements performed without any specific goal. Weaving: obvious lateral swaying, movement of head, neck, forequarters and sometimes hindquarters. Cribbing and windsucking: in cribbing, the horse grasps a fixed object with its incisors, pulls back and draws air into oesophagus. Windsucking is a similar behaviour but without grasping an object. Head shaking and nodding: repetitive bobbing of the head up and down or recurrent and sudden bouts of head tossing. Tongue play: the tongue is pulled out of the mouth and makes twisted movements in the air. The observations made in the present study did not look for possible causes for the different forms of stereotypies observed. Learning test (see also Wolff and Hausberger, 1996). The learning task involved opening a wooden chest to acquire food. The chest measured 60 cm wide 50 cm deep 40 cm high and was closed with a 2 hinge lid. For a period of several days before the experiment began, the chest was put close to the window of the horses’ box so that the animals could see and sniff it but not manipulate it. This was done to avoid fearful reactions to object. For the tests, the chest was placed in the horse’s box near the trough and received a volume of 0.5 l of food (usual pellets). Tests were conducted 90–15 min before the usual feeding time. The ability to learn was measured in time required to perform the task. We measured the latency between the first physical contact of the horse with the chest and eating out of the chest after having successfully opened it by raising the lid with the nose. The horses were offered a maximum of three trials: before the first trial, the experimenter performed the task in front of the horse being tested and showed the food. The horse was then released and observed for 3 min. If it was unsuccessful, the experimenter performed the task again and let the animal sniff the food while halter restrained. It was then released and observed for 3 min. If the animal was still unsuccessful, the procedure was repeated, but this time the horse could take a mouthful of pellets and it was again observed for 3 min. Three trials were allowed for this study and the unsuccessful animals were given the maximum time of 540 s. This procedure has proved useful for discriminating among individuals in their learning abilities in a series of studies (Le Scolan et al., 1997; Hausberger et al., 2004). 2.3. Statistical analysis Non-parametric statistical analyses were used with an accepted p level at 0.05. Mann–Whitney Utests were used in order to compare the behaviour and performances of stereotypic and non-stereotypic horses. Spearman test correlations were conducted in order to seek out potential relations between
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behaviours. x2-Tests allowed us to evaluate possible differences in the number of horses performing successfully the task between groups.
3. Results Amongst the 70 horses, 51 clearly showed stereotypic behaviour both in August and November (1–5% of the time budget, =3.54 1.79). This very high rate did reflect unsuitable environmental conditions (Hausberger et al., in preparation). Scan sampling performed in November revealed also that stereotypic animals spent less time lying down (Mann–Whitney Utest: U = 892.5 p = 0.048) and sleeping (U = 529 p = 0.0001) than the non-stereotypic horses. There was no correlation, however, between the time spent in stereotypic behaviour and the time spent sleeping (Spearman test: p > 0.05), which is not surprising given the low interindividual variation in the time spent in stereotypies (see above).
Fig. 1. (a) Time required (mean S.E.) to open the chest by stereotypic and non-stereotypic horses respectively submitted to an instrumental task. Three trials of 3 min were allowed. If unsuccessful, a maximum time of 540 s was given. Their tendency to perform stereotypies had been assessed by observations in the box, independently of the task. ** Mann–Whitney U-test: p < 0.02. (b) Percentage of unsuccessful animals (%) to open the chest in stereotypic and nonstereotypic horses respectively. **x2-Test: p < 0.02.
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As a whole, more (36 out of 51) stereotypic animals than non-stereotypic animals (3 out of 19) were unsuccessful in opening the chest within the three trials allowed (x2 = 5.16, p < 0.02). Moreover stereotypic horses appeared to require more time in order to perform the task ðX ¼ 368:64 215:03 sÞ as compared to non-stereotypic animals ðX ¼ 220:84 203:03 sÞ (n1 = 51, n2 = 19, U = 365, p = 0.011) (Fig. 1). No difference in performance appeared according to the type of stereotypy performed (x2-test, p > 0.05 in all cases). 4. Discussion This study shows for the first time that motor stereotypies and learning impairments are related in an animal species. Stereotypic horses clearly required more time to learn an instrumental task than non-stereotypic horses. This finding raises important questions both in terms of the processes involved and in terms of horses’ use. Three lines of processes can be considered: cortisol related effects, endorphin related effects and attentional disorders. The relation between an increase in plasma cortisol levels and stereotypic behaviour has not been clearly shown in horses and the results are rather contradictory (McBride, 1996; McGreevy and Nicol, 1998; Pell and McGreevy, 1999; McBride and Cuddeford, 2001), which is also the case in cattle (Redbo, 1993, 1998) and pigs (Dantzer et al., 1987). Moreover, the relation between cortisol levels, learning and memory is unclear as it depends on the kind of events that have to be memorized, on the cortisol concentration before and after learning and also on the balance between catecholamines and cortisol (Al’Absi et al., 2002; Abercrombie et al., 2003; Sauro et al., 2003; Cain et al., 2004; Buss et al., 2004; Lupien et al., 2005). Cortisol is therefore probably not the proximal factor involved. Stereotypies have been sometimes associated with high plasma endorphin levels in horses (Lebelt et al., 1998; McGreevy and Nicol, 1998) and in other species (Cronin et al., 1985) although large variations appear between studies. Heritability of the propensity to perform stereotypies in horses is supposed to rely upon a higher sensitivity of opiate receptors (Pell and McGreevy, 1999). Endorphins may be involved both in terms of plasma levels, reflecting then the release of pituitary endorphin in the blood as a HPA stress response, and in the brain as high levels of endorphins (or opioids) in basal ganglia are associated with the onset and maintenance of stereotypic behaviours (Nistico et al., 1981). Both responses are separated by the brain–blood barrier. Since opioids are supposed to have a general negative effect on learning (Hoyamoun et al., 2003; Guarna et al., 2004), an impact of endorphins may explain our results. The structures involved in horses are not known but the mesoaccumbens and nigrostriatal systems are implicated in stereotypies in other animals (Cabib et al., 1998). Basal ganglia seem to be involved in stereotypies of animals as well as in several motor disorders in humans (Nurnberg et al., 1997; Powell et al., 1999; Garner et al., 2003). While only one study seems to find a relation between learning and motor disorders in children (Mahone et al., 2004), the tics and compulsive disorders observed in the Tourette syndrome seem to be associated with learning disabilities (Gilles de la Tourette, 1889; Burd et al., 1992; Leckman, 2002; Marsh et al., 2004). These disorders result from a dysfunction of basal ganglia (Fattaposta et al., 2005; Singer, 2005). Our results suggest that further questioning should involve attentional processes and a possible decrease of attention related to stereotypies. The findings that stereotypic horses did not lie down and sleep as much as non-stereotypic animals suggest that they may be focusing on their stereotyped behaviours. Such animals may not be able any more to put their attention to new stimuli. This may also be related to a certain tiredness (lower time sleeping and energy spent in
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repetitive movements), but also to a loss of interest. Lower motivational levels as well as tiredness do not promote learning new tasks. The importance of sleep for memory (Karni et al., 1994; Peigneux et al., 2001) and plasticity (Frank et al., 2001) is well known while sleep problems may lead to behavioural disorders in humans (Zuckerman et al., 1987). The importance of sleep and attention in the link between stereotypies and learning is therefore a further promising line. Finally, this study raises important questions concerning the horses’ use in terms of performance. The findings that learning abilities are impaired in stereotypic horses have important implications and deserves further consideration. Whether or not this effect is mediated by a lower attention, it may be important for riders and especially trainers to be aware that stereotypic horses may need more patience and time in order to learn new tasks. The instrumental task we used has been shown to correlate with evaluations of learning abilities at work in horses (Le Scolan et al., 1997). In view of these findings, more consideration should be given to the performances of stereotypic horses (Miller, 2005). Acknowledgments This study could be performed thanks to the permission of Lieutenant Colonel d’He´rouville and the help of P. Galloux at the ‘‘ Ecole Nationale d’Equitation de Saumur ’’. We are grateful to Prof. S. Tordjman for useful comments and C. Lunel for his help in preparing the manuscript. References Abercrombie, H.C., Kalin, N.H., Thurow, M.E., Rosenkranz, M.A., Davidson, R.J., 2003. Cortisol variation in humans affects memory for emotionally laden and neutral information. Behav. Neurosci. 117, 505–516. Al’Absi, M., Hugdahl, K., Lovallo, W.R., 2002. Adrenocortical stress responses and altered working memory performance. Psychophysiology 39, 95–99. Altman, J., 1974. Observational study of behaviour: sampling methods. Behaviour 19, 227–267. Burd, L., Kauffman, D.W., Kerbeshian, J., 1992. Tourette syndrome and learning disabilities. J. Learn Disabil. 25, 598– 604. Buss, C., Wolf, O.T., Witt, J., Hellhammer, D.H., 2004. Autobiographic memory impairement following acute cortisol administration. Psychoneuroendocrinology 29, 1093–1096. Cabib, S., Giardino, L., Calza, L., Zanni, M., Mele, A., Pulisiallegra, S., 1998. Stress promotes major changes in dopamine receptors densities within the mesoaccumbens and nigrostriatal systems. Neuroscience 84, 193–200. Cain, S.W., Karatsoros, I., Gautam, N., Konar, Y., Funk, D., McDonald, R.J., Ralph, M.R., 2004. Blunted cortisol rhythm is associated with learning impairment in aged hamsters. Physiol. Behav. 82, 339–344. Callard, M.D., Bursten, S.N., Price, E.O., 2000. Repetitive backflipping behaviour in captive roof rats (Rattus rattus) and the effects of cage enrichment. Anim. Welfare 9, 139–152. Cooper, J.J., Nicol, C.J., 1996. Stereotypic behaviour in wild caught and laboratory bred bank voles (Clethrinomys glareolus). Anim. Welfare 5, 245–257. Cooper, J.J., McDonald, L., Mills, D.S., 2000. The effect of increasing visual horizons on stereotypic weaving: implications for the social housing of stabled horses. Appl. Anim. Behav. Sci. 69, 67–83. Cronin, G.M., Wiepkema, P.R., van Ree, J.M., 1985. Endogenous opioids are involved in abnormal stereotyped behaviours of tethered sows. Neuropeptides 6 (6), 527–530. Dantzer, R., Gonyou, H.W., Curtis, S.E., Kelley, K.W., 1987. Changes in serum cortisol reveal functionnal differences in frustration-induced chain chewing in pigs. Physiol. Behav. 39, 775–777. Fattaposta, F., Restuccia, R., Colonnese, C., Labruna, L., Gareffa, G., Bianco, F., 2005. Gilles de la Tourette syndrome and voluntary movement: a functionnal MRI study. Psychiatr. Res.: Neuroimag. 138, 269–272. Frank, M.G., Issa, N.P., Stryker, M.P., 2001. Sleep enhances plasticity in the developing visual cortex. Neuron 30, 275– 287. Garner, J.P., Meehan, C.L., Mench, J.A., 2003. Stereotypies in caged parrots, schizophrenia and autism: evidence for a common mechanism. Behav. Brain Res. 145 (1/2), 125–134.
M. Hausberger et al. / Applied Animal Behaviour Science 107 (2007) 299–306
305
Gilles de la Tourette, G., 1889. La maladie des tics convulsifs. La Semaine Medicale 19, 153–156. Guarna, M., Ghelardini, C., Galeotti, N., Bartolini, A., Noli, L., Neri, C., Stefano, G.B., Bianchi, E., 2004. Effects of endogenous morphine deprivation on memory retention of passive avoidance learning in mice. Int. J. Neuropsychopharmacol. 7, 311–319. Hausberger, M., Richard, M.A., 2005. Individual differences in the domestic horse, origins,development and stability. In: Mills, D.S., McDonnell, S.M. (Eds.), The Domestic Horse. Cambridge University Press, Cambridge, pp. 33–52. Hausberger, M., Bruderer, C., Le Scolan, N., Pierre, J.S., 2004. The interplay of environmental and genetic factors in temperament/personality traits of horses. J. Comp. Psychol. 118, 434–446. Houpt, K.A., McDonnell, S.M., 1993. Equine stereotypies. Compend. Cont. Educ. Practis. Veterin. 15, 1265–1272. Hoyamoun, H., Khavandgar, S., Zarrindast, M.R., 2003. Morphine state-dependent learning: interactions with alpha2adrenoreceptors and acute stress. Behav. Pharmacol. 14, 41–48. Karni, A., Taune, D., Rubenstein, B.S., Askenasy, J.J., Sagi, D., 1994. Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265, 679–682. Le Scolan, N., Hausberger, M., Wolff, A., 1997. Stability over situations in temperamental traits of horses as revealed by experimental and scoring approaches. Behav. Process. 41, 257–266. Lebelt, D., Zanella, A.J., Unshelm, J., 1998. Physiological correlates associated with cribbing behavior in horses: changes in thermal threshold, heart rate, plasma-endorphin and serotonin. Equine Clin. Behav. 27, 21–27. Leckman, J.F., 2002. Tourette’s syndrome. Lancet 360 (9345), 1577–1586. Luescher, U.A., McKeown, D.B., Halip, J., 1991. Reviewing the causes of obsessive disorders in horses. Vet. Med. 86, 527–530. Luescher, U.A., McKeown, D.B., Dean, H., 1998. A cross-sectional study on compulsive behaviour (stable vices) in horses. Equine Vet. J. 27 (Suppl.), 14–18. Lupien, S.J., Fiocco, A., Wan, N., Maheu, F., Lord, C., Schramek, T., Tu, M.T., 2005. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30, 225–242. Mahone, E.M., Dana Bridges, R.N., Prahme, C., Singer, H.S., 2004. Repetitive arm and hand movements (complex motor stereotypies) in children. J. Pediatrics 145, 391–395. Marsh, R., Alexander, G.M., Packard, M.G., Zhu, H., Wingard, J.C., Quackenbush, G., Peterson, B.S., 2004. Habit learning in Tourette syndrome: a translational neuroscience approach to a developmental psychopathology. Arch. Gen. Psychiatr. 61, 1259–1268. McBride, S.D., 1996. A comparison of physical and pharmacological treatments for stereotypic befaviour in the horse. In: Duncan, I.J.H., Widowski, T.M., Haley, D.B. (Eds.), Proceedings of the 30th International Congress for the International, Guelph: Centre for the Study of Animal Welfare. Society of Applied Ethology, p. 26. McBride, S.D., Cuddeford, D., 2001. The putative welfare-reducing effects of preventing equine stereotypic behaviour. Anim. Welfare 10, 173–189. McGreevy, P., Nicol, C., 1998. Physiological and behavioral consequences associated with short-term prevention of cribbiting in horses. Physiol. Behav. 65, 15–23. McGreevy, P.D., Cripps, P.J., French, N.P., Green, L.E., Nicol, C.J., 1995. Management factors associated with stereotypic and redirected behaviour in the thoroughbred horse. Equine Vet. J. 27, 86–91. Mills, D.S., 2005. Repetitive movement problems in the horse. In: Mills, D.S., McDonnell, S.M. (Eds.), The Domestic Horse. Cambridge University Press, Cambridge, pp. 212–227. Mills, D.S., Macleod, C.A., 2002. The response of crib-biting and windsucking in horses to dietary supplementation with an antacid mixture. Ippologia 13, 33–41. Nistico, G., Stephenson, J.D., Montanini, S., Marmo, E., 1981. Behavioral and electrocortical effects of beta-endorphin after intracerebral infusion in rats. J. Med. 12, 463–474. Nurnberg, H.G., Keith, S.J., Paxton, D.M., 1997. Consideration of the relevance of ethological animal models for human repetitive behavioral spectrum disorders. Biol. Psychiatr. 41, 226–229. ¨ dberg, F.O., 1986. The jumping stereotypy in the bank vole (Clethrionomys glareolus). Biol. Behav. 11, 130–143. O Peigneux, P., Laureys, S., Delbeuck, X., Maquet, P., 2001. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport 12, 111–124. Pell, S.M., McGreevy, P.D., 1999. A study of cortisol and beta-endorphin levels in stereotypic and normal thoroughbreds. Appl. Anim. Behav. Sci. 64, 81–90. Powell, S.B., Newmann, H.A., Pendergast, J.F., Lewis, M.H., 1999. A rodent model of spontaneous stereotypy: initial characterization of developmental, environmental and neurobiological factors. Physiol. Behav. 66, 355–363. Redbo, I., 1993. Stereotypies and cortisol secretion in heifers subjected to tethering. Appl. Anim. Behav. Sci. 3, 213–225. Redbo, I., 1998. Relations between oral stereotypies, open-field behavior and pituitary–adrenal system in growing dairy cattle. Physiol. Behav. 64, 273–278.
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Rushen, J., De passille, A.M., Schouten, W., 1990. Stereotypic behavior, endogenous opioids and posfeeding hypoalgesia in pigs. Physiol. Behav. 48, 91–96. Sauro, M.D., Jorgensen, R.S., Pedlow, C.T., 2003. Stress, glucocorticoids and memory: a meta-analytic review. Stress 6, 235–245. Singer, H.S., 2005. Tourette’s syndrome: from behaviour to biology. Lancet Neurol. 4, 149–159. Wiepkema, P.R., Schouten, W.G., 1992. Stereotypies in sows during chronic stress. Psychother. Psychosom. 57, 194–199. Wolff, A., Hausberger, M., 1996. Learning and memorisation of two different tasks in horses: the effects of age, sex and sire. Appl. Anim. Behav. Sci. 46, 137–143. Wu¨rbel, H., Stauffacher, M., vonHolst, D., 1996. Stereotypies in laboratory mice-quantative and qualitative description of the ontogeny of ‘‘wire-gnawing’’ and ‘‘jumping’’ in Zur:ICR and Zur:ICR nu. Ethology 102, 371–385. Zuckerman, B., Stevenson, J., Bailey, V., 1987. Sleep problems in early childhood: continuities, predictive factors and behavioral correlates. Pediatrics 80, 664–671.
Lower learning abilities in stereotypic horses Martine Hausberger *, Emmanuel Gautier, Christine Mu¨ller, Patrick Jego UMR 6552 CNRS Ethologie, Evolution, Ecologie, Universite´ de Rennes 1, Campus de Beaulieu, 35042 Rennes Cedex, France Accepted 5 October 2006 Available online 13 November 2006
Abstract The question of whether motor stereotypies may be associated with learning disorders is a highly debated issue both in humans and animals, but evidence is still scarce. The aim of the present study was to investigate the relation between the occurrence of stereotypic behaviours in horses where stereotypies are well described and learning abilities measurable. Seventy horses were observed in their box at two periods (August and November) and were then submitted to an instrumental task (opening a chest by raising the lid using the nose). Fifty-one of them had shown stereotypic behaviours at both periods. It appeared that more stereotypic horses (36/51) were unsuccessful than non-stereotypic horses (3/19) in the learning task. When successful, they required a longer time in order to perform the task (368 s on average against 220 for the nonstereotypic horses). No difference was found according to the type of stereotypy performed. This is to our knowledge the first time that a relation is found between stereotypy and learning in an animal species. The additional finding that stereotypic horses spent less time lying down and sleeping suggests a possible role of attentional processes. This finding has important implications for the horse industry. # 2006 Published by Elsevier B.V. Keywords: Stereotypies; Learning ability; Horses
1. Introduction The question of whether motor stereotypies may be associated with learning disorders is a highly debated issue, especially in humans, but evidence is still scarce. Mahone et al. (2004) found that 20% of children with motor complex stereotypies exhibited a learning disability. * Corresponding author. Tel.: +33 2 23 23 69 28; fax: +33 2 23 23 69 27. E-mail address: [email protected] (M. Hausberger). 0168-1591/$ – see front matter # 2006 Published by Elsevier B.V. doi:10.1016/j.applanim.2006.10.003
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Patients with Tourette syndrome show learning disabilities (Burd et al., 1992; Marsh et al., 2004) as a result of basal ganglia deficits (Fattaposta et al., 2005; Singer, 2005). However to what extent motor and learning disorders are related remains an important issue. The development of animal models would certainly lead to a better understanding of these phenomena (Marsh et al., 2004), but evidence is scarce here too. The existence of motor disorders, commonly called stereotypies, is well known in captive and ¨ dberg, 1986; Cooper and Nicol, 1996; Wu¨rbel et al., 1996; domestic animals: rodents, birds (O Powell et al., 1999; Callard et al., 2000) but also farm animals (cattle: Redbo, 1993, 1998; pigs: Cronin et al., 1985; Rushen et al., 1990; Wiepkema and Schouten, 1992). This phenomenon receives particular attention in horses, as these behaviours are undesirable for owners and may lead to physiological problems. In horses, repetive movements without any specific goal have been defined as stereotypies (Houpt and McDonnell, 1993), obsessive-compulsive or compulsive disorders (Luescher et al., 1991, 1998; review in Mills, 2005). They tend to appear in unfavourable conditions (McGreevy et al., 1995) in predisposed animals (Hausberger and Richard, 2005). Stereotypies tend to be associated with higher endorphin levels (McGreevy and Nicol, 1998; Pell and McGreevy, 1999). Whether or not learning abilities or performance are impaired in these animals is not known (Mills, 2005). In the present study, we investigated the relation between the occurrence of stereotypic behaviours in individual horses and their ability to learn a task. Observations of the behaviour of 70 horses in their box let us identify ‘‘stable stereotypic’’ horses (stereotypies were present both in two periods separated by a 3 month interval) and non-stereotypic horses. We then submitted both categories of horses to a learning test that correlates with learning abilities in the working situation (Le Scolan et al., 1997). 2. Materials and methods 2.1. Animals and observation procedures Seventy seven French saddlebred horses were observed at the ‘‘Ecole Nationale d’Equitation’’ at Saumur (France) at two time periods: August and November. They were 4–15-year old geldings and were all housed in the same conditions: single box housing (3.30 m 3.40 m), 1 h riding everyday (see Table 1). They were fed pellets and hay twice a day and had water ad libitum. Only the animals that showed stereotypic (or no stereotypic) behaviour consistently at the two time periods were kept for the study, which corresponded to 70 horses. The seven others were only performing stereotypies in November. The analyses included evaluations of individual stereotypies and an analysis of pooled data. Horses were observed in their box using two different methods, with the aim of ensuring that the animal really belonged to one or the other category: Table 1 Type of work performed by the horses observed in their box and tested in the learning task (number of horses)
All horses Stereotypic
Jumping
Eventing
Instruction
Voltige
Dressage
High school
21 16
8 3
12 7
5 2
20 15
11 8
High school horses are dressage horses at a more sophisticated level of performance (elevated paces). The work of the voltige horses differs from the other categories: the horses are lunged on a circle and the riders jump on the back and perform gymnastic movements.
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In the August session, focal sampling was used: all behaviours of the focal animal were recorded continuously during sessions of 5 min. Observations were made at three time periods: 8–11 a.m., 1–4 p.m. and 5–7 p.m. Meals were distributed between 6.30 and 7 a.m. and 4.15–6.30 p.m. All horses were observed 10 times (=50 min total/horse), covering the three daily sessions that included time periods before and after the meals (favourable for observing repetitive movements: Cooper et al., 2000; Mills and Macleod, 2002). In the November session, observations were made using instantaneous scan sampling (Altman, 1974): each horse was observed in sessions of 5 min with behaviour being recorded every 10 s. Each horse was observed four times at the same daily periods as in August. A total of 120 scans were obtained for each horse (20 min). All observations in the box were made by a single observer. To control for differences in learning abilities between (dressage + high school) and (eventing + jumping) horses (Hausberger et al., 2004), the ratio of stereotypic horses was approximately equal in each category (23/31 and 19/29). 2.2. Terminology The stereotypic behaviours noted corresponded to those described in a variety of studies (review in Mills, 2005) and had the common feature of consisting of minor repetitive movements performed without any specific goal. Weaving: obvious lateral swaying, movement of head, neck, forequarters and sometimes hindquarters. Cribbing and windsucking: in cribbing, the horse grasps a fixed object with its incisors, pulls back and draws air into oesophagus. Windsucking is a similar behaviour but without grasping an object. Head shaking and nodding: repetitive bobbing of the head up and down or recurrent and sudden bouts of head tossing. Tongue play: the tongue is pulled out of the mouth and makes twisted movements in the air. The observations made in the present study did not look for possible causes for the different forms of stereotypies observed. Learning test (see also Wolff and Hausberger, 1996). The learning task involved opening a wooden chest to acquire food. The chest measured 60 cm wide 50 cm deep 40 cm high and was closed with a 2 hinge lid. For a period of several days before the experiment began, the chest was put close to the window of the horses’ box so that the animals could see and sniff it but not manipulate it. This was done to avoid fearful reactions to object. For the tests, the chest was placed in the horse’s box near the trough and received a volume of 0.5 l of food (usual pellets). Tests were conducted 90–15 min before the usual feeding time. The ability to learn was measured in time required to perform the task. We measured the latency between the first physical contact of the horse with the chest and eating out of the chest after having successfully opened it by raising the lid with the nose. The horses were offered a maximum of three trials: before the first trial, the experimenter performed the task in front of the horse being tested and showed the food. The horse was then released and observed for 3 min. If it was unsuccessful, the experimenter performed the task again and let the animal sniff the food while halter restrained. It was then released and observed for 3 min. If the animal was still unsuccessful, the procedure was repeated, but this time the horse could take a mouthful of pellets and it was again observed for 3 min. Three trials were allowed for this study and the unsuccessful animals were given the maximum time of 540 s. This procedure has proved useful for discriminating among individuals in their learning abilities in a series of studies (Le Scolan et al., 1997; Hausberger et al., 2004). 2.3. Statistical analysis Non-parametric statistical analyses were used with an accepted p level at 0.05. Mann–Whitney Utests were used in order to compare the behaviour and performances of stereotypic and non-stereotypic horses. Spearman test correlations were conducted in order to seek out potential relations between
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behaviours. x2-Tests allowed us to evaluate possible differences in the number of horses performing successfully the task between groups.
3. Results Amongst the 70 horses, 51 clearly showed stereotypic behaviour both in August and November (1–5% of the time budget, =3.54 1.79). This very high rate did reflect unsuitable environmental conditions (Hausberger et al., in preparation). Scan sampling performed in November revealed also that stereotypic animals spent less time lying down (Mann–Whitney Utest: U = 892.5 p = 0.048) and sleeping (U = 529 p = 0.0001) than the non-stereotypic horses. There was no correlation, however, between the time spent in stereotypic behaviour and the time spent sleeping (Spearman test: p > 0.05), which is not surprising given the low interindividual variation in the time spent in stereotypies (see above).
Fig. 1. (a) Time required (mean S.E.) to open the chest by stereotypic and non-stereotypic horses respectively submitted to an instrumental task. Three trials of 3 min were allowed. If unsuccessful, a maximum time of 540 s was given. Their tendency to perform stereotypies had been assessed by observations in the box, independently of the task. ** Mann–Whitney U-test: p < 0.02. (b) Percentage of unsuccessful animals (%) to open the chest in stereotypic and nonstereotypic horses respectively. **x2-Test: p < 0.02.
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As a whole, more (36 out of 51) stereotypic animals than non-stereotypic animals (3 out of 19) were unsuccessful in opening the chest within the three trials allowed (x2 = 5.16, p < 0.02). Moreover stereotypic horses appeared to require more time in order to perform the task ðX ¼ 368:64 215:03 sÞ as compared to non-stereotypic animals ðX ¼ 220:84 203:03 sÞ (n1 = 51, n2 = 19, U = 365, p = 0.011) (Fig. 1). No difference in performance appeared according to the type of stereotypy performed (x2-test, p > 0.05 in all cases). 4. Discussion This study shows for the first time that motor stereotypies and learning impairments are related in an animal species. Stereotypic horses clearly required more time to learn an instrumental task than non-stereotypic horses. This finding raises important questions both in terms of the processes involved and in terms of horses’ use. Three lines of processes can be considered: cortisol related effects, endorphin related effects and attentional disorders. The relation between an increase in plasma cortisol levels and stereotypic behaviour has not been clearly shown in horses and the results are rather contradictory (McBride, 1996; McGreevy and Nicol, 1998; Pell and McGreevy, 1999; McBride and Cuddeford, 2001), which is also the case in cattle (Redbo, 1993, 1998) and pigs (Dantzer et al., 1987). Moreover, the relation between cortisol levels, learning and memory is unclear as it depends on the kind of events that have to be memorized, on the cortisol concentration before and after learning and also on the balance between catecholamines and cortisol (Al’Absi et al., 2002; Abercrombie et al., 2003; Sauro et al., 2003; Cain et al., 2004; Buss et al., 2004; Lupien et al., 2005). Cortisol is therefore probably not the proximal factor involved. Stereotypies have been sometimes associated with high plasma endorphin levels in horses (Lebelt et al., 1998; McGreevy and Nicol, 1998) and in other species (Cronin et al., 1985) although large variations appear between studies. Heritability of the propensity to perform stereotypies in horses is supposed to rely upon a higher sensitivity of opiate receptors (Pell and McGreevy, 1999). Endorphins may be involved both in terms of plasma levels, reflecting then the release of pituitary endorphin in the blood as a HPA stress response, and in the brain as high levels of endorphins (or opioids) in basal ganglia are associated with the onset and maintenance of stereotypic behaviours (Nistico et al., 1981). Both responses are separated by the brain–blood barrier. Since opioids are supposed to have a general negative effect on learning (Hoyamoun et al., 2003; Guarna et al., 2004), an impact of endorphins may explain our results. The structures involved in horses are not known but the mesoaccumbens and nigrostriatal systems are implicated in stereotypies in other animals (Cabib et al., 1998). Basal ganglia seem to be involved in stereotypies of animals as well as in several motor disorders in humans (Nurnberg et al., 1997; Powell et al., 1999; Garner et al., 2003). While only one study seems to find a relation between learning and motor disorders in children (Mahone et al., 2004), the tics and compulsive disorders observed in the Tourette syndrome seem to be associated with learning disabilities (Gilles de la Tourette, 1889; Burd et al., 1992; Leckman, 2002; Marsh et al., 2004). These disorders result from a dysfunction of basal ganglia (Fattaposta et al., 2005; Singer, 2005). Our results suggest that further questioning should involve attentional processes and a possible decrease of attention related to stereotypies. The findings that stereotypic horses did not lie down and sleep as much as non-stereotypic animals suggest that they may be focusing on their stereotyped behaviours. Such animals may not be able any more to put their attention to new stimuli. This may also be related to a certain tiredness (lower time sleeping and energy spent in
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repetitive movements), but also to a loss of interest. Lower motivational levels as well as tiredness do not promote learning new tasks. The importance of sleep for memory (Karni et al., 1994; Peigneux et al., 2001) and plasticity (Frank et al., 2001) is well known while sleep problems may lead to behavioural disorders in humans (Zuckerman et al., 1987). The importance of sleep and attention in the link between stereotypies and learning is therefore a further promising line. Finally, this study raises important questions concerning the horses’ use in terms of performance. The findings that learning abilities are impaired in stereotypic horses have important implications and deserves further consideration. Whether or not this effect is mediated by a lower attention, it may be important for riders and especially trainers to be aware that stereotypic horses may need more patience and time in order to learn new tasks. The instrumental task we used has been shown to correlate with evaluations of learning abilities at work in horses (Le Scolan et al., 1997). In view of these findings, more consideration should be given to the performances of stereotypic horses (Miller, 2005). Acknowledgments This study could be performed thanks to the permission of Lieutenant Colonel d’He´rouville and the help of P. Galloux at the ‘‘ Ecole Nationale d’Equitation de Saumur ’’. We are grateful to Prof. S. Tordjman for useful comments and C. Lunel for his help in preparing the manuscript. References Abercrombie, H.C., Kalin, N.H., Thurow, M.E., Rosenkranz, M.A., Davidson, R.J., 2003. Cortisol variation in humans affects memory for emotionally laden and neutral information. Behav. Neurosci. 117, 505–516. Al’Absi, M., Hugdahl, K., Lovallo, W.R., 2002. Adrenocortical stress responses and altered working memory performance. Psychophysiology 39, 95–99. Altman, J., 1974. Observational study of behaviour: sampling methods. Behaviour 19, 227–267. Burd, L., Kauffman, D.W., Kerbeshian, J., 1992. Tourette syndrome and learning disabilities. J. Learn Disabil. 25, 598– 604. Buss, C., Wolf, O.T., Witt, J., Hellhammer, D.H., 2004. Autobiographic memory impairement following acute cortisol administration. Psychoneuroendocrinology 29, 1093–1096. Cabib, S., Giardino, L., Calza, L., Zanni, M., Mele, A., Pulisiallegra, S., 1998. Stress promotes major changes in dopamine receptors densities within the mesoaccumbens and nigrostriatal systems. Neuroscience 84, 193–200. Cain, S.W., Karatsoros, I., Gautam, N., Konar, Y., Funk, D., McDonald, R.J., Ralph, M.R., 2004. Blunted cortisol rhythm is associated with learning impairment in aged hamsters. Physiol. Behav. 82, 339–344. Callard, M.D., Bursten, S.N., Price, E.O., 2000. Repetitive backflipping behaviour in captive roof rats (Rattus rattus) and the effects of cage enrichment. Anim. Welfare 9, 139–152. Cooper, J.J., Nicol, C.J., 1996. Stereotypic behaviour in wild caught and laboratory bred bank voles (Clethrinomys glareolus). Anim. Welfare 5, 245–257. Cooper, J.J., McDonald, L., Mills, D.S., 2000. The effect of increasing visual horizons on stereotypic weaving: implications for the social housing of stabled horses. Appl. Anim. Behav. Sci. 69, 67–83. Cronin, G.M., Wiepkema, P.R., van Ree, J.M., 1985. Endogenous opioids are involved in abnormal stereotyped behaviours of tethered sows. Neuropeptides 6 (6), 527–530. Dantzer, R., Gonyou, H.W., Curtis, S.E., Kelley, K.W., 1987. Changes in serum cortisol reveal functionnal differences in frustration-induced chain chewing in pigs. Physiol. Behav. 39, 775–777. Fattaposta, F., Restuccia, R., Colonnese, C., Labruna, L., Gareffa, G., Bianco, F., 2005. Gilles de la Tourette syndrome and voluntary movement: a functionnal MRI study. Psychiatr. Res.: Neuroimag. 138, 269–272. Frank, M.G., Issa, N.P., Stryker, M.P., 2001. Sleep enhances plasticity in the developing visual cortex. Neuron 30, 275– 287. Garner, J.P., Meehan, C.L., Mench, J.A., 2003. Stereotypies in caged parrots, schizophrenia and autism: evidence for a common mechanism. Behav. Brain Res. 145 (1/2), 125–134.
M. Hausberger et al. / Applied Animal Behaviour Science 107 (2007) 299–306
305
Gilles de la Tourette, G., 1889. La maladie des tics convulsifs. La Semaine Medicale 19, 153–156. Guarna, M., Ghelardini, C., Galeotti, N., Bartolini, A., Noli, L., Neri, C., Stefano, G.B., Bianchi, E., 2004. Effects of endogenous morphine deprivation on memory retention of passive avoidance learning in mice. Int. J. Neuropsychopharmacol. 7, 311–319. Hausberger, M., Richard, M.A., 2005. Individual differences in the domestic horse, origins,development and stability. In: Mills, D.S., McDonnell, S.M. (Eds.), The Domestic Horse. Cambridge University Press, Cambridge, pp. 33–52. Hausberger, M., Bruderer, C., Le Scolan, N., Pierre, J.S., 2004. The interplay of environmental and genetic factors in temperament/personality traits of horses. J. Comp. Psychol. 118, 434–446. Houpt, K.A., McDonnell, S.M., 1993. Equine stereotypies. Compend. Cont. Educ. Practis. Veterin. 15, 1265–1272. Hoyamoun, H., Khavandgar, S., Zarrindast, M.R., 2003. Morphine state-dependent learning: interactions with alpha2adrenoreceptors and acute stress. Behav. Pharmacol. 14, 41–48. Karni, A., Taune, D., Rubenstein, B.S., Askenasy, J.J., Sagi, D., 1994. Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265, 679–682. Le Scolan, N., Hausberger, M., Wolff, A., 1997. Stability over situations in temperamental traits of horses as revealed by experimental and scoring approaches. Behav. Process. 41, 257–266. Lebelt, D., Zanella, A.J., Unshelm, J., 1998. Physiological correlates associated with cribbing behavior in horses: changes in thermal threshold, heart rate, plasma-endorphin and serotonin. Equine Clin. Behav. 27, 21–27. Leckman, J.F., 2002. Tourette’s syndrome. Lancet 360 (9345), 1577–1586. Luescher, U.A., McKeown, D.B., Halip, J., 1991. Reviewing the causes of obsessive disorders in horses. Vet. Med. 86, 527–530. Luescher, U.A., McKeown, D.B., Dean, H., 1998. A cross-sectional study on compulsive behaviour (stable vices) in horses. Equine Vet. J. 27 (Suppl.), 14–18. Lupien, S.J., Fiocco, A., Wan, N., Maheu, F., Lord, C., Schramek, T., Tu, M.T., 2005. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30, 225–242. Mahone, E.M., Dana Bridges, R.N., Prahme, C., Singer, H.S., 2004. Repetitive arm and hand movements (complex motor stereotypies) in children. J. Pediatrics 145, 391–395. Marsh, R., Alexander, G.M., Packard, M.G., Zhu, H., Wingard, J.C., Quackenbush, G., Peterson, B.S., 2004. Habit learning in Tourette syndrome: a translational neuroscience approach to a developmental psychopathology. Arch. Gen. Psychiatr. 61, 1259–1268. McBride, S.D., 1996. A comparison of physical and pharmacological treatments for stereotypic befaviour in the horse. In: Duncan, I.J.H., Widowski, T.M., Haley, D.B. (Eds.), Proceedings of the 30th International Congress for the International, Guelph: Centre for the Study of Animal Welfare. Society of Applied Ethology, p. 26. McBride, S.D., Cuddeford, D., 2001. The putative welfare-reducing effects of preventing equine stereotypic behaviour. Anim. Welfare 10, 173–189. McGreevy, P., Nicol, C., 1998. Physiological and behavioral consequences associated with short-term prevention of cribbiting in horses. Physiol. Behav. 65, 15–23. McGreevy, P.D., Cripps, P.J., French, N.P., Green, L.E., Nicol, C.J., 1995. Management factors associated with stereotypic and redirected behaviour in the thoroughbred horse. Equine Vet. J. 27, 86–91. Mills, D.S., 2005. Repetitive movement problems in the horse. In: Mills, D.S., McDonnell, S.M. (Eds.), The Domestic Horse. Cambridge University Press, Cambridge, pp. 212–227. Mills, D.S., Macleod, C.A., 2002. The response of crib-biting and windsucking in horses to dietary supplementation with an antacid mixture. Ippologia 13, 33–41. Nistico, G., Stephenson, J.D., Montanini, S., Marmo, E., 1981. Behavioral and electrocortical effects of beta-endorphin after intracerebral infusion in rats. J. Med. 12, 463–474. Nurnberg, H.G., Keith, S.J., Paxton, D.M., 1997. Consideration of the relevance of ethological animal models for human repetitive behavioral spectrum disorders. Biol. Psychiatr. 41, 226–229. ¨ dberg, F.O., 1986. The jumping stereotypy in the bank vole (Clethrionomys glareolus). Biol. Behav. 11, 130–143. O Peigneux, P., Laureys, S., Delbeuck, X., Maquet, P., 2001. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport 12, 111–124. Pell, S.M., McGreevy, P.D., 1999. A study of cortisol and beta-endorphin levels in stereotypic and normal thoroughbreds. Appl. Anim. Behav. Sci. 64, 81–90. Powell, S.B., Newmann, H.A., Pendergast, J.F., Lewis, M.H., 1999. A rodent model of spontaneous stereotypy: initial characterization of developmental, environmental and neurobiological factors. Physiol. Behav. 66, 355–363. Redbo, I., 1993. Stereotypies and cortisol secretion in heifers subjected to tethering. Appl. Anim. Behav. Sci. 3, 213–225. Redbo, I., 1998. Relations between oral stereotypies, open-field behavior and pituitary–adrenal system in growing dairy cattle. Physiol. Behav. 64, 273–278.
306
M. Hausberger et al. / Applied Animal Behaviour Science 107 (2007) 299–306
Rushen, J., De passille, A.M., Schouten, W., 1990. Stereotypic behavior, endogenous opioids and posfeeding hypoalgesia in pigs. Physiol. Behav. 48, 91–96. Sauro, M.D., Jorgensen, R.S., Pedlow, C.T., 2003. Stress, glucocorticoids and memory: a meta-analytic review. Stress 6, 235–245. Singer, H.S., 2005. Tourette’s syndrome: from behaviour to biology. Lancet Neurol. 4, 149–159. Wiepkema, P.R., Schouten, W.G., 1992. Stereotypies in sows during chronic stress. Psychother. Psychosom. 57, 194–199. Wolff, A., Hausberger, M., 1996. Learning and memorisation of two different tasks in horses: the effects of age, sex and sire. Appl. Anim. Behav. Sci. 46, 137–143. Wu¨rbel, H., Stauffacher, M., vonHolst, D., 1996. Stereotypies in laboratory mice-quantative and qualitative description of the ontogeny of ‘‘wire-gnawing’’ and ‘‘jumping’’ in Zur:ICR and Zur:ICR nu. Ethology 102, 371–385. Zuckerman, B., Stevenson, J., Bailey, V., 1987. Sleep problems in early childhood: continuities, predictive factors and behavioral correlates. Pediatrics 80, 664–671.